Bacteriocins as promising antimicrobial peptides, definition, classification, and their potential applications in cheeses

Abstract

There is increased importance to finding alternative solutions to antibiotic resistance which require more research, bacteriocins are promising antimicrobial peptides with inhibitory and bactericidal activities that might be one of these solutions. Bacteriocins are small antimicrobial peptides synthesized by bacterial ribosomes, active against the bacterial pathogen, multidrug-resistant bacteria, and cancer therapy. Lactic acid bacteria (LAB) are one of the most used bacteria to produce bacteriocins and dairy products (i.e. cheeses) consider rich sources of LAB isolates. Enterococcus faecalis, Lactobacillus fermentum, L. plantarum, L. helveticus, L. pentosus, L. paracasei subsp. paracasei, L. rhamnosus I, and L. delbrueckii subsp. lactis are strong strains in bacteriocins production. Several applications were applied to control bacterial pathogens spread in cheeses, one of them is using bacteriocins and bacteriocins-like inhibitory substances (BLIS). To reduce foodborne pathogens and spoilage bacteria in cheese, bacteriocins can be applied in several means such as inoculating cheese with bacteriocin-producer strain and adding purified or semi-purified bacteriocin as a food additive. This review is focused on bacteriocins and BLIS classification, mechanism, and applications in dairy products i.e. cheeses.

Keywords:
bacteriocins; antimicrobials; Lactic acid bacteria; foodborne pathogens; cheese

1 Introduction

The antimicrobial activity of bacteriocins has promising potential in inhibiting and killing bacterial pathogens (Pato et al., 2022a). Bacteriocins are antimicrobial peptides synthesized by bacterial ribosomes, with bacteriostatic or bactericidal effects against pathogens (Simons et al., 2020). It could be produced by gram-positive and gram-negative bacteria. They are mostly used in the food industry as natural bio preservatives instead of chemical preservatives to protect products from spoilage and pathogenic bacteria (Todorov et al., 2019; Pato et al., 2022b; Barboza et al., 2022). Bacteriocins-like inhibitory substances (BLIS) are also ribosomally synthesized peptides that possess abilities like bacteriocin but have not been yet characterized for their amino acid sequence (Caulier et al., 2019). Nisin is the first approved bacteriocin used as a food preservative (Khelissa et al., 2021). Lactic acid bacteria (LAB) are one of the most used bacteria to produce bacteriocins and BLIS (Tankoano et al., 2019; Jawan et al., 2021; Tang et al., 2022).

Foodborne diseases are a real threat to consumer health, especially in sensitive highly perishable dairy products such as cheeses (Cheng et al., 2022). Since cheeses are rich in various nutrient values which provide an optimum environment for pathogenic bacteria that escape during the manufacturing process or survive in retail stores (Kaur & Kaur, 2021). As a result of the widespread of antibiotic-resistant bacteria due to the overuse of antibiotics, there is a requirement for effective therapeutic approaches to control the spread of resistance (Soltani et al., 2021).

LAB and their bacteriocins are considered safe and useful food additives to control the growth of pathogens and spoilage microorganisms in foods (Mokoena et al., 2021). Nisin, Pediocin PA-1, and Micocin are the only FDA-approved bacteriocins to use as food preservatives since they inhibit the growth of many gram-positive bacteria and food-borne pathogens (Naskar & Kim, 2021). Bacteriocin of lactobacillus plantarum isolated from a Tulum cheese reduced the growth of Staphylococcus aureus during production and ripening of white-brined cheeses (Taban et al., 2019). L. Plantarum ST71KS isolated from Bulgarian goat milk feta cheese was able to produce class IIa bacteriocin that had a bactericidal effect on Listeria monocytogenes (Martinez et al., 2013). Pediocin PA-1 gene was detected in pediococcus pentosaceus isolated from ripened Minas cheese, an artisanal cheese made with raw cow’s milk (Gutiérrez-Cortés et al., 2018). Several applications were applied to control bacterial pathogens spread in cheeses, one of them is using bacteriocins and bacteriocins-like inhibitory substances (BLIS). This review is focus on bacteriocins and BLIS classification, mechanism, and applications in dairy products i.e. cheeses.

2 Bacteriocin and Bacteriocins Like Inhibitory Substances (BLIS)

Bacteriocin is a small proteinaceous compound with low-molecular-mass, consists of 30 to 60 amino acids synthesized by bacterial ribosomes, heat-stable at 100 °C for 10 min, and extracellularly excreted to inhibit or kill other bacterial strains (Mokoena, 2017; Raval et al., 2020; Moradi et al., 2021). Normally not termed antibiotics to avoid confusion with therapeutic antibiotics (Sen & Ray, 2019) rapidly digested by proteases in the human digestive tract which is the difference between them and most therapeutic antibiotics (Tkhruni et al., 2020).

Bacteriocins have a narrow or wide spectrum via inhibiting taxonomically close bacteria, or a wide variety of bacteria (Silva et al., 2018). Bacteriocins have a different spectrum of activity, mode of action, molecular weight (MW), genetic origin, and biochemical properties (Darbandi et al., 2022) BLIS are antimicrobial peptides produced by LAB that possess bacteriocin ability, but that have not yet been characterized for their amino acid sequence (El-Gendy et al., 2021) Recently, BLIS gained interest due to their potential use as natural antimicrobial peptides that inhibit the growth of pathogenic and contaminant bacteria in several applications such as food, clinical, veterinary, and others (Agriopoulou et al., 2020; Hefzy et al., 2021; Hu et al., 2018).

BLIS activity can also be measured by various methods such as agar well diffusion assay, spot-on-lawn assay, turbidimetric assay, ELISA, radiometry, conductance measurements, and bioassays based on self-induction skills (Sidek et al., 2018; Zou et al., 2018; Arakawa, 2019). The most widely used assay is the determination method that exhibits the growth inhibition potential of a bacteriocin (Sidek et al., 2018). The physical and chemical properties of BLIS are important, especially in the food industry because of the complexity of food processing (Yi et al., 2022).

3 Bacteriocins of Lactic Acid Bacteria (LAB)

LAB are non-spore-forming bacteria, gram-positive, anaerobic but aerotolerant rods or cocci, catalase-negative, and fastidious bacteria, with a high tolerance for low pH, ferment carbohydrates to produce energy and lactic acid as the primary product of fermentation (Gupta et al., 2018; Miranda et al., 2021; Wang et al., 2021). Moreover, it is produced antimicrobial substances such as bacteriocins, BLIS, hydrogen peroxide, organic acids, diacetyl, acetoin, and antifungal peptides (Egan et al., 2016). LAB produce a large number of bacteriocins from strains like Lactobacillus, Pediococcus, Lactococcus, and Enterococcus (Trejo-González et al., 2021).

LAB bacteriocins are often active at various pH values, resistant to high temperatures, and active against plenty of food pathogenic and spoilage bacteria (Ahmad et al., 2017). Furthermore, bacteriocins produced by LAB are sensitive to digestive enzymes such as pancreatin complex, trypsin, and chymotrypsin, and for this reason, has no impact negatively on the gut microbiota (Egan et al., 2016) Lactobacillus and their bacteriocins have been used in food preservation, and to control human pathogens (Mokoena et al., 2021).

4 Bacteriocins classification

Based on the biosynthesis mechanism and biological activity of bacteriocins, it's classified into three major classes: Class I - small post-translationally modified peptides with molecular mass < 5 kDa, class II - unmodified peptides with molecular mass 6-10 kDa and including or not stabilizing disulfide bridges and class III - larger peptides [> 10 kDa, thermo-labile; Negash & Tsehai (2020); Zimina et al. (2020)].

Class I Bacteriocins/Lantibiotics are heat-stable small peptides (< 5 kDa) and are subdivided into two types based on charge difference (Negash & Tsehai, 2020). It is highly posttranslational modified and contains characteristic polycyclic thioether amino acids such as lanthionine, methyl-lanthionine (Veettil & Chitra, 2022), and unsaturated amino acids such as dehydroalanine and 2-amino isobutyric acid (Roy et al., 2018). Type A-lantibiotics are flexible screw-shaped molecules with a positive charge of 2-4 kDa. Effect on the cell membrane by forming pores which lead to depolarization of the target species cytoplasmic membranes such as nisin and lacticin 3147 (Negash & Tsehai, 2020). Type B-lantibiotics are globular peptides 2-3 kDa, without net charge or negative charge, that interfere with cellular enzymatic reactions of sensitive bacteria cell wall synthesis, such as Mersacidin (Moravej et al., 2018)

Class II Bacteriocins are small heat-stable peptides (< 10 kDa) with amphiphilic helical structures that allow them to insert into the membrane of the target cell which leads to cell depolarization and death (Negash & Tsehai, 2020). In addition, it is non-lanthionine-containing peptides that are not modified after translation beyond the elimination of a leader peptide and the formation of a conserved N-terminal disulfide bridge (Kozic et al., 2018). Subclass IIa peptides are monomers and have an N-terminal consensus sequence Tyr-Gly-Asn-Gly-Val-Xaa-Cys. They are active against L. monocytogenes such as pediocin PA-1 and sakacin A. Subclass IIb with two-component bacteriocins in which two distinct peptides act synergistically to generate an antimicrobial effect such as lactation F and lactococci G (Negash & Tsehai, 2020). Subclass IIc has circular bacteriocins carrying two transmembrane segments that facilitate pore formation in the target cell such as gassericin A, circularin A, and carnocyclin A (Yaghoubi et al., 2020).

Class III Bacteriocins are peptides with high molecular weight (> 30 kDa), and heat-labile proteins (Yaghoubi et al., 2020). In addition, it includes three groups bacteriolysins, non-lytic bacteriocins, and tailocins. Bacteriolysins are large lytic polypeptides that target the peptidoglycan layer such as lysostaphin, zoocin A, millericin B, and enterolisin A. Non-lytic bacteriocins are large non-lytic polypeptides, their mechanism of action is not based on cell wall lysis, it is believed that blocking the absorption of glucose and its inclusion in cellular macromolecules leads to carbohydrate starvation that kills the target cell such as helveticin J and casecin 80. The last one are tailocins which is multiprotein complex, with structure like a phage tail that target the lipopolysaccharides such as diffocin and monocin (Zimina et al., 2020).

5 Bacteriocins: mechanisms of action

Bacteriocins inhibit the growth of target organisms in different mechanisms. There is a mechanism that can function primarily on the cell envelope and other mechanisms are primarily active in the cell by affecting gene expression and protein production (Negash & Tsehai, 2020). Bacteriocins have bactericidal effects that may be accompanied with or without cell lysis (Qiao et al., 2021). It produced from LAB mostly inhibits gram-positive bacteria and exerts its antibacterial effect by targeting the cell envelope-associated mechanisms (Rahmeh et al., 2020). Lantibiotics and some class II of bacteriocins target lipid II and eliminate the synthesis of peptidoglycan (Negash & Tsehai, 2020).

Other bacteriocins use lipid II as a docking molecule to start pore formation which resulted in variation of the cytoplasm membrane potential and finally, cell death (Du et al., 2018). Nisin, the most studied bacteriocin is capable of both mechanisms (Kumariya et al., 2019). Lactococcin A is a class II bacteriocin that targets the cell by binding to the pore-forming receptor mannose phosphotransferase system [Man-PTS; Daba et al. (2018)].

Some bacteriocins show antimicrobial activity by their enzymatic activities, such as colicin E2 showing DNase activity, colicin E3 showing RNase activity, and megalin A-216 showing phospholipase activity against the target organism (Negash & Tsehai, 2020). Class II of peptides due to their structure can be inserted into the membrane of the target cell, causing depolarization and death. On the other hand, class III bacteriocins directly function on the cell wall of gram-positive resulting in cell death-like lysostaphin (Baindara et al., 2018; Negash & Tsehai, 2020).

The bactericidal mode of action of recombinant bacteriocin BMP32r against gram-positive and gram-negative bacteria was similar with slightly different. Cell damage was observed such as cell membrane disruption, intracellular material outflow, and even cell lysis in Escherichia coli after being treated with BMP32r (Qiao et al., 2020). Several bacteriocins inhibit gram-negative bacteria by interfering with their nucleic acids, and protein metabolism. For example, MccJ25 inhibits RNA polymerase, microcin B17 (MccB17) inhibits DNA gyrase, and MccC7-C51 inhibits aspartyl-tRNA synthetase. In addition, MccE492 as an exception works by pore formation (Cotter et al., 2013).

6 Application of bacteriocins

Bacteriocins are promising antimicrobial peptides with potential applications in different sectors such as food, clinical health, and others.

6.1 Food industry

Bacteriocins got the attention as natural antimicrobial agents to use in food as preservatives instead of chemical preservatives (Gokoglu, 2019). Usually, their application includes the use of bacteriocin-producer strain as inoculation of food, adding purified or semi-purified bacteriocin as a food additive, and using a previously fermented product with a bacteriocin-producing strain during food processing as an ingredient (Barcenilla et al., 2022).

Nisin, Pediocin PA-1, and Micocin are the only FDA-approved bacteriocins to use as food preservatives, by inhibiting the growth of many gram-positive bacteria and food-borne pathogens such as L. monocytogenes (Naskar & Kim, 2021). Applied mostly in dairy products and canned food, especially in processed cheese protect the product from heat-resistant spore-forming bacteria such as Bacillus and Clostridium (Anumudu et al., 2021).

Bacteriocins are colorless, odorless, and tasteless so, it is a perfect solution for food products without changing their properties (Negash & Tsehai, 2020). Moreover, they are stable at high temperatures, low pH, and a wide range of salt concentrations (Yang et al., 2018; Costa et al., 2019).

There are several advantages of using bacteriocins as food preservatives included increase food shelf life, reducing the transmission of risky foodborne pathogens via food, offering more protection during thermal conditions, lowering the economic losses due to food spoilage and outbreaks, and applying less severe treatment to food during processing to keep nutrients values and properties of food product without change (Reinseth et al., 2020).

Despite these advantages, we should keep in mind the addition of specific bacteriocins to food products could be limited by a narrow, limited spectrum of activity (Reinseth et al., 2020) or to the hydrophobic nature of used bacteriocin which may lead to the separation of organic fat within the food matrix (Khelissa et al., 2021). In addition, uneven distribution or poor solubility of bacteriocin may affect the antimicrobial activity of these molecules. Using bacteriocins in combination with other preservation methods may increase their antibacterial activity (Soltani et al., 2021).

Due to the interaction with food components or inactivation by proteolytic enzymes, nisin loses its activity easily, and to overcome this problem encapsulation of nisin Z in liposomes improves the inhibitory action and stability in the cheddar cheese matrix (Kaur & Kaur, 2021). Also, encapsulation of nisin with alginate/resistant starch increased its efficiency in cheddar cheese, Clostridium tyrobutyricum count was reduced after one week and inhibited completely after four weeks (Hassan et al., 2020).

7 Bacteriocins produced by LAB isolated from cheeses

Bacteriocin production can be obtained by any type of bacteria. Table 1 shows examples of several bacteriocins produced from LAB isolated from cheeses and their activity against foodborne pathogens. Five strains of LAB i.e. Lactococcus lactis IMAU32258, L. garvieae JB2826472, Enterococcus durans FMA8, E. faecium L3-23, E. faecium IMAU9421 were isolated from Carpathian cheese as cell-free supernatant (CFS) without any addition of hydrogen peroxide or adjusted pH value. The antagonistic activity of the bacteriocins LAB against pathogenic was studied by Musiy et al. (2020). They found that E. durans FMA8 had the highest activity against S. typhimurium PCM 2182, followed by L. monocytogenes PCM 2191, E. coli PCM 2208, and S. aureus PCM 458. Similarly, L. lactis IMAU32258 bacteriocins had the highest activity against S. typhimurium PCM 2182, followed by E. coli PCM 2208, L. monocytogenes PCM 2191, and S. aureus PCM 458. However, a bacteriocin from L. garvieae showed the lowest antagonistic activity against studied pathogenic bacteria. Surprisingly, the LAB cultures of the isolates demonstrated higher antagonistic activity towards these tested pathogens as compared to their bacteriocins. Moreover, Margalho et al. (2020) used different types of cheese to isolate LAB bacteriocins. Among 27 isolates, five isolates had a strong inhibitory effect (Table 1). L. plantarum (1QB314) bacteriocin isolated from Colonial cheese showed an ability to inhibit the growth of all tested pathogens (S. aureus FRI S6, S. aureus FRI 361, L. monocytogenes ATCC 3968, and L. monocytogenes ATCC 3973). In addition, several bacteriocins were also produced from Lb. plantarum 1QB77 (Minas artisanal cheeses), lactobacillus sp. 3QB167 (Manteiga cheese), L.lactis 1QB167 (Manteiga cheese), and lactobacillus sp. 1QB459 (Caipira cheese) which showed varied in their inhibition activity. The treated bacteriocins with enzymes such as protease, α-chymotrypsin, proteinase K, and trypsin showed strong inhibition against tested pathogens with no zone of inhibition were observed. E. faecalis KT11 bacteriocin obtained from traditional Kargı Tulum cheese was tested against several pathogens and had the highest inhibition activity against the growth of Serratia marcescens NRRL 2544, S. aureus ATCC 25923, M. luteus NRRL 1018, Bacillus subtilis NRRL NRS 744, Enterobacter aerogenes ATCC 13048, L. monocytogenes LMG 13305 and Klebsiella pneumoniae ATCC 13883, respectively. Moreover, bacteriocin treated with pepsin and α-amylase had a significant (p< 0.05) inhibition activity against Pseudomonas aeruginosa ATCC 2783, M. luteus NRRL 1018, and S. aureus ATCC 25923. In contrast, P. aeruginosa ATCC 2783 and M. luteus NRRL 1018 bacteriocins had similar inhibition activity (16.0 ± 0.5 mm) when treated with catalase (Abanoz & Kunduhoglu, 2018).

Table 1
Activity of bacteriocins isolated from lactic acid bacteria of different types of cheeses.

Cheese	Technique	Bacteriocins LAB strain	Pathogenic strain	Inhibition zone (mm)	Control	Inhibition zone (mm)	p value	References
Traditional Kargı Tulum cheese	Agar well diffusion assay	Enterococcus faecalis KT11	Klebsiella pneumoniae ATCC 13883	14.0 ± 0.8	CSF	N.M.	p < 0.05	Abanoz & Kunduhoglu, 2018
			Serratia marcescens NRRL 2544	18.0 ± 0.6		N.M.
			Enterobacter aerogenes ATCC 13048	15.0 ± 0.8		N.M.
			Pseudomonas aeruginosa ATCC 2783	14.0 ± 1.0		18.0 ± 1.0
			Listeria monocytogenes LMG 13305	15.0 ± 0.5		N.M.
			Bacillus subtilis NRRL NRS 744	15.0 ± 0.8		N.M.
			M. luteus NRRL 1018	16.0 ± 1.6		15.0 ± 0.8
			Staphylococcus aureus ATCC 25923	16.0 ± 1.8		15.0 ± 0.5
Mongolian Fermented Cheese	Oxford cup assay	L. plantarum KLDS 1.0344	Escherichia coli ATCC 43889	(+++)*	Sterile water	N.D.	p < 0.05	Muhammad et al., 2019
			Salmonella typhimurium ATCC 14028	(+++)*
			Staphylococcus aureus ATCC 25923	(+++)*
			Listeria monocytogenes ATCC 19115	(++)*
Traditional cheese samples	Agar well diffusion assay	Lactiplantibacillus plantarum	Listeria monocytogenes ATCC 7644	86.60%	N.D.	N.D.	N.M.	Afshari et al., 2022
			Staphylococcus aureus PTCC 1431	80%
			Salmonella typhimurium ATCC 14028	93.30%
			Pseudomonas aeruginosa ATCC 9027	73.30%
			Escherichia coli PTCC 1338	66.60%
		Lactobacillus rhamnosus	Listeria monocytogenes ATCC 7644	80%
			Staphylococcus aureus PTCC 1431	93.30%
			Salmonella typhimurium ATCC 14028	86.60%
			Pseudomonas aeruginosa ATCC 9027	100%
			Escherichia coli PTCC 1338	93.30%
		Limosilactobacillus fermentum	Listeria monocytogenes ATCC 7644	100%
			Staphylococcus aureus PTCC 1431	93.30%
			Salmonella typhimurium ATCC 14028	86.60%
			Pseudomonas aeruginosa ATCC 9027	93.30%
			Escherichia coli PTCC 1338	86.60%
Carpathian cheese	Agar well diffusion assay	L. lactis IMAU32258	S. aureus PCM 458	8.4 ± 1.3	Bacteriocins producing culture	20.2 ± 2.8	p < 0.05	Musiy et al., 2020
			L. monocytogenes PCM 2191	17.1 ± 1.2		18.5 ± 1.6
			S. typhimurium PCM 2182	18.9 ± 0.6		24.1 ± 1.9
			E. coli PCM 2208	17.3 ± 2.1		18.7 ± 1.6
		L. garvieae JB282647 2	S. aureus PCM 458	6.3 ± 0.9		8.4 ± 1.1
			L. monocytogenes PCM 2191	6.2 ± 0.4		10.2 ± 0.9
			S. typhimurium PCM 2182	7.4 ± 1.3		9.5 ± 1.4
			E. coli PCM 2208	7.1 ± 1.3		8.4 ± 0.7
		E. faecium IMAU9421	S. aureus PCM 458	6.1 ± 0.6		18.1 ± 1.4
			L. monocytogenes PCM 2191	14.3 ± 2.1		14.4 ± 1.3
			S. typhimurium PCM 2182	15.7 ± 1.7		20.3 ± 1.7
			E. coli PCM 2208	16.5 ± 1.5		23.6 ± 2.4
		E. faecium L3-23	S. aureus PCM 458	10.2 ± 1.7		19.5 ± 1.6
			L. monocytogenes PCM 2191	18.5 ± 1.7		21.4 ± 0.8
			S. typhimurium PCM 2182	20.1 ± 2.5		25.2 ± 1.2
			E. coli PCM 2208	18.4 ± 2.7		20.1 ± 1.2
		E. durans FMA8	S. aureus PCM 458	12.5 ± 2.9		20.6 ± 2.1
			L. monocytogenes PCM 2191	22.6 ± 1.8		23.6 ± 1.3
			S. typhimurium PCM 2182	23.8 ± 1.2		24.0 ± 0.9
			E. coli PCM 2208	20.4 ± 1.4		20.3 ± 1.9
Minas artisanal cheeses	Agar well diffusion assay	Lb. plantarum 1QB77	S. aureus FRI S6	inhibited	CSF	N.D.	p < 0.05	Margalho et al., 2020
			S. aureus FRI 361	no zone was observed
			L. monocytogenes ATCC 3968	inhibited
			L. monocytogenes ATCC 3973	inhibited
Manteiga		lactobacillus sp. 3QB167	S. aureus FRI S6	inhibited
			S. aureus FRI 361	no zone was observed
			L. monocytogenes ATCC 3968	inhibited
			L. monocytogenes ATCC 3973	inhibited
Manteiga		L.lactis 1QB167	S. aureus FRI S6	inhibited
			S. aureus FRI 361	no zone was observed
			L. monocytogenes ATCC 3968	inhibited
			L. monocytogenes ATCC 3973	inhibited
Caipira		lactobacillus sp. 1QB459	S. aureus FRI S6	inhibited
			S. aureus FRI 361	no zone was observed
			L. monocytogenes ATCC 3968	inhibited
			L. monocytogenes ATCC 3973	inhibited
Colonial		Lb. plantarum 1QB314	S. aureus FRI S6	inhibited
			S. aureus FRI 361	inhibited
			L. monocytogenes ATCC 3968	inhibited
			L. monocytogenes ATCC 3973	inhibited
white cheese	Agar spot and well diffusion assay	E. faecium S1113	E. coli ATCC 25922	(++)ǂ	Bacteriocins producing culture	(+++)ǂ	p < 0.05	Mohammed & Çon, 2021
			B. cereus NRRL B-3711	(+++)ǂ		(+++)ǂ
		E. durans S092	E. coli ATCC 25922	(++)ǂ		(++)ǂ
			B. cereus NRRL B-3711	(+++)ǂ		(+++)ǂ
		E. gallinarum S142	E. coli ATCC 25922	(++)ǂ		(+++)ǂ
			B. cereus NRRL B-3711	(++)ǂ		(+++)ǂ
		L. pentosus S056	E. coli ATCC 25922	(+)ǂ		(+++)ǂ
			B. cereus NRRL B-3711	(+)ǂ		(+++)ǂ
		E. durans S1121	E. coli ATCC 25922	(+++)ǂ		(+++)ǂ
			B. cereus NRRL B-3711	(++)ǂ		(+++)ǂ

• ^*
  +++ (> 10 mm), ++ (5-10 mm).
• ^ǂ
  + (0.5-10 mm), ++ (11-19 mm).
• ⁺
  ++ (> 20 mm); CSF = Cell-free supernatant; N.D. = Not detected; N.M. = Not mentioned.

L. plantarum KLDS 1.0344 bacteriocins isolated from Mongolian fermented cheese was tested against four pathogens, three of them had an inhibition zone larger than 10 mm for E. coli ATCC 43889, Salmonella typhimurium ATCC 14028, and S. aureus ATCC 25923 (Muhammad et al., 2019). However, L. monocytogenes ATCC 19115 had an inhibition zone between 5-10 mm. In addition, L. plantarum KLDS 1.0344 bacteriocins were treated with several factors such as pH, temperature, and enzymes (pepsin and protease). Bacteriocins treated with pepsin and protease have antagonistic activity against S. aureus ATCC 25923 with inhibition zone 18.5 ± 0.8 mm and 20.4 ± 0.8 mm, respectively whereas L. monocytogenes ATCC 19115 had the lowest activity [12.7 ± 0.5 and 14.5 ± 0.5 mm, respectively; Muhammad et al. (2019)]. All tested pathogens had the same inhibition zone of 100.0 ± 0.0 mm when treated with Mongolian fermented cheese bacteriocin at different temperatures (80 °C and 100 °C) and times (20, 30, and 40 min). In addition, the authors reported that antagonistic activity of L. monocytogenes was significantly (p < 0.05) enhanced when the temperature increased to 120 °C for 20 and 40 min (85.0 ± 0.7 and 61.2 ± 0.1 mm, respectively). On the other hand, lower activity towards E. coli was noticed at 120 °C for 20 and 40 min (81.0 ± 0.2 and 40.5 ± 0.0 mm; respectively). Furthermore, bacteriocin's treated at different pH values had the highest inhibition zone (p < 0.05) at pH 2 and the lowest at pH 6 against all tested pathogens (Muhammad et al., 2019). Recently, Lactiplantibacillus plantarum, L. rhamnosus, and Limosilactobacillus fermentum bacteriocins isolated from traditional cheese samples were found to have the highest inhibition zone activity against S. typhimurium ATCC 14028 (93.30%), P. aeruginosa ATCC 9027 (100%), and L. monocytogenes ATCC 7644 (100%); respectively (Afshari et al., 2022). Mohammed & Çon (2021) have investigated five bacteriocins isolated from LAB of white cheese (E. faecium S1113, E. durans S092, E. gallinarum S142, L. pentosus S056, and E. durans S1121). Both E. faecium S1113 and E. durans S092 had a positive effect on B. cereus NRRL B-3711 (> 20 mm) whereas E. durans S1121 affected significantly (p < 0.05) on E. coli ATCC 25922. In addition, the antagonistic activity against these two pathogens significantly improved when pH ranged between 3 - 9.5 with an inhibition zone (0.5-10 mm). All bacteriocins produced from the five isolates inhibited the growth of the tested pathogens with zones ranging from 0.5 to 10 mm (Mohammed & Çon, 2021).

8 Conclusion

Bacteriocins obtained from LAB have strong antimicrobial activity against bacterial pathogens, which makes them a promising alternative to antibiotics. Based on previously bacteriocins research, several strains of LAB-producing bacteriocins isolated from various types of cheese showed high inhibitory activity towards foodborne bacteria such as L. monocytogenes, S. aureus, E. coli, and others. L. plantarum bacteriocins were among the most studied bacteriocins against both gram-positive and gram-negative bacteria. More studies must be conducted to determine the best type of cheese that produce the most effective bacteriocin. Furthermore, bacteriocins differ in their inhibitory effect, so there is a need to find more bacteriocins with a broad spectrum against foodborne bacteria to be used as a food preservative to eliminate the growth of undesirable bacteria in cheese.

• Practical Application: Bacteriocins obtained from LAB have strong antimicrobial activity against bacterial pathogens, which makes them a promising alternative to antibiotics.

References

• Abanoz, H. S., & Kunduhoglu, B. (2018). Antimicrobial activity of a bacteriocin produced by Enterococcus faecalis KT11 against some pathogens and antibiotic-resistant bacteria. Korean Journal for Food Science of Animal Resources, 38(5), 1064-1079. http://dx.doi.org/10.5851/kosfa.2018.e40 PMid:30479512.
  » http://dx.doi.org/10.5851/kosfa.2018.e40
• Afshari, A., Hashemi, M., Tavassoli, M., Eraghi, V., & Noori, S. M. A. (2022). Probiotic bacteria from 10 different traditional Iranian cheeses: isolation, characterization, and investigation of probiotic potential. Food Science & Nutrition, 10(6), 2009-2020. http://dx.doi.org/10.1002/fsn3.2817 PMid:35702287.
  » http://dx.doi.org/10.1002/fsn3.2817
• Agriopoulou, S., Stamatelopoulou, E., Sachadyn-Król, M., & Varzakas, T. (2020). Lactic acid bacteria as antibacterial agents to extend the shelf life of fresh and minimally processed fruits and vegetables: quality and safety aspects. Microorganisms, 8(6), 952. http://dx.doi.org/10.3390/microorganisms8060952 PMid:32599824.
  » http://dx.doi.org/10.3390/microorganisms8060952
• Ahmad, V., Khan, M. S., Jamal, Q. M. S., Alzohairy, M. A., Karaawi, M. A., & Siddiqui, M. U. (2017). Antimicrobial potential of bacteriocins: in therapy, agriculture and food preservation. International Journal of Antimicrobial Agents, 49(1), 1-11. http://dx.doi.org/10.1016/j.ijantimicag.2016.08.016 PMid:27773497.
  » http://dx.doi.org/10.1016/j.ijantimicag.2016.08.016
• Anumudu, C., Hart, A., Miri, T., & Onyeaka, H. (2021). Recent advances in the application of the antimicrobial peptide nisin in the inactivation of spore-forming bacteria in foods. Molecules, 26(18), 5552. http://dx.doi.org/10.3390/molecules26185552 PMid:34577022.
  » http://dx.doi.org/10.3390/molecules26185552
• Arakawa, K. (2019). Basic antibacterial assay to screen for bacteriocinogenic lactic acid bacteria and to elementarily characterize their bacteriocins. Methods in Molecular Biology, 1887, 15-22. http://dx.doi.org/10.1007/978-1-4939-8907-2_2 PMid:30506245.
  » http://dx.doi.org/10.1007/978-1-4939-8907-2_2
• Baindara, P., Korpole, S., & Grover, V. (2018). Bacteriocins: perspective for the development of novel anticancer drugs. Applied Microbiology and Biotechnology, 102(24), 10393-10408. http://dx.doi.org/10.1007/s00253-018-9420-8 PMid:30338356.
  » http://dx.doi.org/10.1007/s00253-018-9420-8
• Barboza, G. R., Almeida, J. M. D., & Silva, N. C. C. (2022). Use of natural substrates as an alternative for the prevention of microbial contamination in the food industry. Food Science and Technology, 42, e05720. http://dx.doi.org/10.1590/fst.05720
  » http://dx.doi.org/10.1590/fst.05720
• Barcenilla, C., Ducic, M., López, M., Prieto, M., & Álvarez-Ordóñez, A. (2022). Application of lactic acid bacteria for the biopreservation of meat products: a systematic review. Meat Science, 183, 108661. http://dx.doi.org/10.1016/j.meatsci.2021.108661 PMid:34467880.
  » http://dx.doi.org/10.1016/j.meatsci.2021.108661
• Caulier, S., Nannan, C., Gillis, A., Licciardi, F., Bragard, C., & Mahillon, J. (2019). Overview of the antimicrobial compounds produced by members of the Bacillus subtilis group. Frontiers in Microbiology, 10, 302. http://dx.doi.org/10.3389/fmicb.2019.00302 PMid:30873135.
  » http://dx.doi.org/10.3389/fmicb.2019.00302
• Cheng, T., Wang, L., Guo, Z., & Li, B. (2022). Technological characterization and antibacterial activity of Lactococcus lactis subsp. cremoris strains for potential use as starter culture for cheddar cheese manufacture. Food Science and Technology, 42, e13022. http://dx.doi.org/10.1590/fst.13022
  » http://dx.doi.org/10.1590/fst.13022
• Costa, R. J., Voloski, F. L., Mondadori, R. G., Duval, E. H., & Fiorentini, Â. M. (2019). Preservation of meat products with bacteriocins produced by lactic acid bacteria isolated from meat. Journal of Food Quality, 2019, 4726510. http://dx.doi.org/10.1155/2019/4726510
  » http://dx.doi.org/10.1155/2019/4726510
• Cotter, P. D., Ross, R. P., & Hill, C. (2013). Bacteriocins - a viable alternative to ntibiotics? Nature Reviews. Microbiology, 11(2), 95-105. http://dx.doi.org/10.1038/nrmicro2937 PMid:23268227.
  » http://dx.doi.org/10.1038/nrmicro2937
• Daba, G. M., Ishibashi, N., Gong, X., Taki, H., Yamashiro, K., Lim, Y. Y., Zendo, T., & Sonomoto, K. (2018). Characterisation of the action mechanism of a Lactococcus-specific bacteriocin, lactococcin Z. Journal of Bioscience and Bioengineering, 126(5), 603-610. http://dx.doi.org/10.1016/j.jbiosc.2018.05.018 PMid:29929768.
  » http://dx.doi.org/10.1016/j.jbiosc.2018.05.018
• Darbandi, A., Asadi, A., Ari, M. M., Ohadi, E., Talebi, M., Zadeh, M. H., Emamie, A. D., Ghanavati, R., & Kakanj, M. (2022). Bacteriocins: properties and potential use as antimicrobials. Journal of Clinical Laboratory Analysis, 36(1), e24093. http://dx.doi.org/10.1002/jcla.24093 PMid:34851542.
  » http://dx.doi.org/10.1002/jcla.24093
• Du, H., Yang, J., Lu, X., Lu, Z., Bie, X., Zhao, H., Zhang, C., & Lu, F. (2018). Purification, characterization, and mode of action of plantaricin GZ1-27, a novel bacteriocin against Bacillus cereus. Journal of Agricultural and Food Chemistry, 66(18), 4716-4724. http://dx.doi.org/10.1021/acs.jafc.8b01124 PMid:29690762.
  » http://dx.doi.org/10.1021/acs.jafc.8b01124
• Egan, K., Field, D., Rea, M. C., Ross, R. P., Hill, C., & Cotter, P. D. (2016). Bacteriocins: novel solutions to age old spore-related problems? Frontiers in Microbiology, 7, 461. http://dx.doi.org/10.3389/fmicb.2016.00461 PMid:27092121.
  » http://dx.doi.org/10.3389/fmicb.2016.00461
• El-Gendy, A. O., Brede, D. A., Essam, T. M., Amin, M. A., Ahmed, S. H., Holo, H., Nes, I. F., & Shamikh, Y. I. (2021). Purification and characterization of bacteriocins-like inhibitory substances from food isolated Enterococcus faecalis OS13 with activity against nosocomial enterococci. Scientific Reports, 11(1), 3795. http://dx.doi.org/10.1038/s41598-021-83357-z PMid:33589735.
  » http://dx.doi.org/10.1038/s41598-021-83357-z
• Gokoglu, N. (2019). Novel natural food preservatives and applications in seafood preservation: a review. Journal of the Science of Food and Agriculture, 99(5), 2068-2077. http://dx.doi.org/10.1002/jsfa.9416 PMid:30318589.
  » http://dx.doi.org/10.1002/jsfa.9416
• Gupta, R., Jeevaratnam, K., & Fatima, A. (2018). Lactic acid bacteria: probiotic characteristic, selection criteria, and its role in human health (a review). International Journal of Emerging Technologies and Innovative Research, 5(10), 411-424.
• Gutiérrez-Cortés, C., Suarez, H., Buitrago, G., Nero, L. A., & Todorov, S. D. (2018). Characterization of bacteriocins produced by strains of Pediococcus pentosaceus isolated from Minas cheese. Annals of Microbiology, 68(6), 383-398. http://dx.doi.org/10.1007/s13213-018-1345-z
  » http://dx.doi.org/10.1007/s13213-018-1345-z
• Hassan, H., Gomaa, A., Subirade, M., Kheadr, E., St-Gelais, D., & Fliss, I. (2020). Novel design for alginate/resistant starch microcapsules controlling nisin release. International Journal of Biological Macromolecules, 153, 1186-1192. http://dx.doi.org/10.1016/j.ijbiomac.2019.10.248 PMid:31756478.
  » http://dx.doi.org/10.1016/j.ijbiomac.2019.10.248
• Hefzy, E. M., Khalil, M., Amin, A., Ashour, H. M., & Abdelaliem, Y. F. (2021). Bacteriocin-like inhibitory substances from probiotics as therapeutic agents for Candida Vulvovaginitis. Antibiotics, 10(3), 306. http://dx.doi.org/10.3390/antibiotics10030306 PMid:33802636.
  » http://dx.doi.org/10.3390/antibiotics10030306
• Hu, J., Ma, L., Nie, Y., Chen, J., Zheng, W., Wang, X., Xie, C., Zheng, Z., Wang, Z., Yang, T., Shi, M., Chen, L., Hou, Q., Niu, Y., Xu, X., Zhu, Y., Zhang, Y., Wei, H., & Yan, X. (2018). A microbiota-derived bacteriocin targets the host to confer diarrhea resistance in early-weaned piglets. Cell Host & Microbe, 24(6), 817-832.e8. http://dx.doi.org/10.1016/j.chom.2018.11.006 PMid:30543777.
  » http://dx.doi.org/10.1016/j.chom.2018.11.006
• Jawan, R., Abbasiliasi, S., Mustafa, S., Kapri, M. R., Halim, M., & Ariff, A. B. (2021). In vitro evaluation of potential probiotic strain Lactococcus lactis Gh1 and its bacteriocin-like inhibitory substances for potential use in the food industry. Probiotics and Antimicrobial Proteins, 13(2), 422-440. http://dx.doi.org/10.1007/s12602-020-09690-3 PMid:32728855.
  » http://dx.doi.org/10.1007/s12602-020-09690-3
• Kaur, R., & Kaur, L. (2021). Encapsulated natural antimicrobials: a promising way to reduce microbial growth in different food systems. Food Control, 123, 107678. http://dx.doi.org/10.1016/j.foodcont.2020.107678
  » http://dx.doi.org/10.1016/j.foodcont.2020.107678
• Khelissa, S., Chihib, N. E., & Gharsallaoui, A. (2021). Conditions of nisin production by Lactococcus lactis subsp. lactis and its main uses as a food preservative. Archives of Microbiology, 203(2), 465-480. http://dx.doi.org/10.1007/s00203-020-02054-z PMid:33001222.
  » http://dx.doi.org/10.1007/s00203-020-02054-z
• Kozic, M., Fox, S. J., Thomas, J. M., Verma, C. S., & Rigden, D. J. (2018). Large scale ab initio modeling of structurally uncharacterized antimicrobial peptides reveals known and novel folds. Proteins, 86(5), 548-565. http://dx.doi.org/10.1002/prot.25473 PMid:29388242.
  » http://dx.doi.org/10.1002/prot.25473
• Kumariya, R., Garsa, A. K., Rajput, Y. S., Sood, S. K., Akhtar, N., & Patel, S. (2019). Bacteriocins: classification, synthesis, mechanism of action and resistance development in food spoilage causing bacteria. Microbial Pathogenesis, 128, 171-177. http://dx.doi.org/10.1016/j.micpath.2019.01.002 PMid:30610901.
  » http://dx.doi.org/10.1016/j.micpath.2019.01.002
• Margalho, L. P., Feliciano, M. D., Silva, C. E., Abreu, J. S., Piran, M. V. F., & Sant’Ana, A. S. (2020). Brazilian artisanal cheeses are rich and diverse sources of nonstarter lactic acid bacteria regarding technological, biopreservative, and safety properties—insights through multivariate analysis. Journal of Dairy Science, 103(9), 7908-7926. http://dx.doi.org/10.3168/jds.2020-18194 PMid:32684468.
  » http://dx.doi.org/10.3168/jds.2020-18194
• Martinez, R. C. R., Wachsman, M., Torres, N. I., LeBlanc, J. G., Todorov, S. D., & Franco, B. D. G. M. (2013). Biochemical, antimicrobial and molecular characterization of a noncytotoxic bacteriocin produced by Lactobacillus plantarum ST71KS. Food Microbiology, 34(2), 376-381. http://dx.doi.org/10.1016/j.fm.2013.01.011 PMid:23541205.
  » http://dx.doi.org/10.1016/j.fm.2013.01.011
• Miranda, C., Contente, D., Igrejas, G., Câmara, S., Dapkevicius, M. D. L. E., & Poeta, P. (2021). Role of exposure to lactic acid bacteria from foods of animal origin in human health. Foods, 10(9), 2092. http://dx.doi.org/10.3390/foods10092092 PMid:34574202.
  » http://dx.doi.org/10.3390/foods10092092
• Mohammed, S., & Çon, A. H. (2021). Isolation and characterization of potential probiotic lactic acid bacteria from traditional cheese. LWT, 152, 112319. http://dx.doi.org/10.1016/j.lwt.2021.112319
  » http://dx.doi.org/10.1016/j.lwt.2021.112319
• Mokoena, M. P. (2017). Lactic acid bacteria and their bacteriocins: classification, biosynthesis and applications against uropathogens: a mini-review. Molecules, 22(8), 1255. http://dx.doi.org/10.3390/molecules22081255 PMid:28933759.
  » http://dx.doi.org/10.3390/molecules22081255
• Mokoena, M. P., Omatola, C. A., & Olaniran, A. O. (2021). Applications of lactic acid bacteria and their bacteriocins against food spoilage microorganisms and foodborne pathogens. Molecules, 26(22), 7055. http://dx.doi.org/10.3390/molecules26227055 PMid:34834145.
  » http://dx.doi.org/10.3390/molecules26227055
• Moradi, M., Molaei, R., & Guimarães, J. T. (2021). A review on preparation and chemical analysis of postbiotics from lactic acid bacteria. Enzyme and Microbial Technology, 143, 109722. http://dx.doi.org/10.1016/j.enzmictec.2020.109722 PMid:33375981.
  » http://dx.doi.org/10.1016/j.enzmictec.2020.109722
• Moravej, H., Moravej, Z., Yazdanparast, M., Heiat, M., Mirhosseini, A., Moghaddam, M. M., & Mirnejad, R. (2018). Antimicrobial peptides: features, action, and their resistance mechanisms in bacteria. Microbial Drug Resistance, 24(6), 747-767. http://dx.doi.org/10.1089/mdr.2017.0392 PMid:29957118.
  » http://dx.doi.org/10.1089/mdr.2017.0392
• Muhammad, Z., Ramzan, R., Abdelazez, A., Amjad, A., Afzaal, M., Zhang, S., & Pan, S. (2019). Assessment of the antimicrobial potentiality and functionality of Lactobacillus plantarum strains isolated from the conventional inner Mongolian fermented cheese against foodborne pathogens. Pathogens, 8(2), 71. http://dx.doi.org/10.3390/pathogens8020071 PMid:31117307.
  » http://dx.doi.org/10.3390/pathogens8020071
• Musiy, L. Y., Tsisaryk, O. Y., Slyvka, I. M., & Kushnir, I. I. (2020). Antagonistic activity of strains of lactic acid bacteria isolated from Carpathian cheese. Regulatory Mechanisms in Biosystems, 11(4), 572-578. http://dx.doi.org/10.15421/022089
  » http://dx.doi.org/10.15421/022089
• Naskar, A., & Kim, K. S. (2021). Potential novel food-related and biomedical applications of nanomaterials combined with bacteriocins. Pharmaceutics, 13(1), 86. http://dx.doi.org/10.3390/pharmaceutics13010086 PMid:33440722.
  » http://dx.doi.org/10.3390/pharmaceutics13010086
• Negash, A. W., & Tsehai, B. A. (2020). Current applications of bacteriocin. International Journal of Microbiology, 2020, 4374891. http://dx.doi.org/10.1155/2020/4374891 PMid:33488719.
  » http://dx.doi.org/10.1155/2020/4374891
• Pato, U., Riftyan, E., Ayu, D. F., Jonnaidi, N. N., Wahyuni, M. S., Feruni, J. A., & Abdel-Wahhab, M. A. (2022a). Antibacterial efficacy of lactic acid bacteria and bacteriocin isolated from Dadih’s against Staphylococcus aureus. Food Science and Technology, 42, e27121. http://dx.doi.org/10.1590/fst.27121
  » http://dx.doi.org/10.1590/fst.27121
• Pato, U., Riftyan, E., Jonnaidi, N. N., Wahyuni, M. S., Feruni, J. A., & Abdel-Wahhab, M. A. (2022b). Isolation, characterization, and antimicrobial evaluation of bacteriocin produced by lactic acid bacteria against Erwinia carotovora. Food Science and Technology, 42, e11922. http://dx.doi.org/10.1590/fst.11922
  » http://dx.doi.org/10.1590/fst.11922
• Qiao, Z., Chen, J., Zhou, Q., Wang, X., Shan, Y., Yi, Y., Liu, B., Zhou, Y., & Lü, X. (2021). Purification, characterization, and mode of action of a novel bacteriocin BM173 from Lactobacillus crustorum MN047 and its effect on biofilm formation of Escherichia coli and Staphylococcus aureus. Journal of Dairy Science, 104(2), 1474-1483. http://dx.doi.org/10.3168/jds.2020-18959 PMid:33246623.
  » http://dx.doi.org/10.3168/jds.2020-18959
• Qiao, Z., Sun, H., Zhou, Q., Yi, L., Wang, X., Shan, Y., Yi, Y., Liu, B., Zhou, Y., & Lü, X. (2020). Characterization and antibacterial action mode of bacteriocin BMP32r and its application as antimicrobial agent for the therapy of multidrug-resistant bacterial infection. International Journal of Biological Macromolecules, 164, 845-854. http://dx.doi.org/10.1016/j.ijbiomac.2020.07.192 PMid:32702420.
  » http://dx.doi.org/10.1016/j.ijbiomac.2020.07.192
• Rahmeh, R., Akbar, A., Alonaizi, T., Kishk, M., Shajan, A., & Akbar, B. (2020). Characterization and application of antimicrobials produced by Enterococcus faecium S6 isolated from raw camel milk. Journal of Dairy Science, 103(12), 11106-11115. http://dx.doi.org/10.3168/jds.2020-18871 PMid:32981738.
  » http://dx.doi.org/10.3168/jds.2020-18871
• Raval, V., Patel, J., Raol, G., Bhavsar, N., Surati, V., Gopani, Y., & Vaidya, Y. (2020). Evaluation of bacteriocin purified from potent lysinibacillussphaericus mk788143 isolated from infant faecal. Journal of Advanced Scientific Research, 11.‏
• Reinseth, I. S., Ovchinnikov, K. V., Tønnesen, H. H., Carlsen, H., & Diep, D. B. (2020). The increasing issue of vancomycin-resistant enterococci and the bacteriocin solution. Probiotics and Antimicrobial Proteins, 12(3), 1203-1217. http://dx.doi.org/10.1007/s12602-019-09618-6 PMid:31758332.
  » http://dx.doi.org/10.1007/s12602-019-09618-6
• Roy, R., Tiwari, M., Donelli, G., & Tiwari, V. (2018). Strategies for combating bacterial biofilms: a focus on anti-biofilm agents and their mechanisms of action. Virulence, 9(1), 522-554. http://dx.doi.org/10.1080/21505594.2017.1313372 PMid:28362216.
  » http://dx.doi.org/10.1080/21505594.2017.1313372
• Sen, C., & Ray, P. R. (2019). Biopreservation of dairy products using bacteriocins. Indian Food Industry, 1(4), 51-60.
• Sidek, N. L. M., Halim, M., Tan, J. S., Abbasiliasi, S., Mustafa, S., & Ariff, A. B. (2018). Stability of bacteriocin-like inhibitory substance (BLIS) produced by Pediococcus acidilactici kp10 at different extreme conditions. BioMed Research International, 2018, 5973484. http://dx.doi.org/10.1155/2018/5973484 PMid:30363649.
  » http://dx.doi.org/10.1155/2018/5973484
• Silva, C. C., Silva, S. P., & Ribeiro, S. C. (2018). Application of bacteriocins and protective cultures in dairy food preservation. Frontiers in Microbiology, 9, 594. http://dx.doi.org/10.3389/fmicb.2018.00594 PMid:29686652.
  » http://dx.doi.org/10.3389/fmicb.2018.00594
• Simons, A., Alhanout, K., & Duval, R. E. (2020). Bacteriocins, antimicrobial peptides from bacterial origin: overview of their biology and their impact against multidrug-resistant bacteria. Microorganisms, 8(5), 639. http://dx.doi.org/10.3390/microorganisms8050639 PMid:32349409.
  » http://dx.doi.org/10.3390/microorganisms8050639
• Soltani, S., Hammami, R., Cotter, P. D., Rebuffat, S., Said, L. B., Gaudreau, H., Bédard, F., Biron, E., Drider, D., & Fliss, I. (2021). Bacteriocins as a new generation of antimicrobials: toxicity aspects and regulations. FEMS Microbiology Reviews, 45(1), fuaa039. http://dx.doi.org/10.1093/femsre/fuaa039 PMid:32876664.
  » http://dx.doi.org/10.1093/femsre/fuaa039
• Taban, B., Çolaklar, M., Aytac, S. A., Özer, H. B., Gursoy, A., & Akcelik, N. (2019). Application of Bacteriocin-Like Inhibitory Substances (BLIS)-producing probiotic strain of Lactobacillus plantarum in control of Staphylococcus aureus in white-brined cheese production. Journal of Agricultural Sciences, 25(4), 401-408.
• Tang, H. W., Phapugrangkul, P., Fauzi, H. M., & Tan, J. S. (2022). Lactic acid bacteria bacteriocin, an antimicrobial peptide effective against multidrug resistance: a comprehensive review. International Journal of Peptide Research and Therapeutics, 28(1), 14. http://dx.doi.org/10.1007/s10989-021-10317-6
  » http://dx.doi.org/10.1007/s10989-021-10317-6
• Tankoano, A., Diop, M. B., Sawadogo-Lingani, H., Mbengue, M., Kaboré, D., Traoré, Y., & Savadogo, A. (2019). Isolation and characterization of lactic acid bacteria producing bacteriocin like inhibitory substance (BLIS) from “Gappal”, a dairy product from Burkina Faso. Advances in Microbiology, 9(4), 343-358. http://dx.doi.org/10.4236/aim.2019.94020
  » http://dx.doi.org/10.4236/aim.2019.94020
• Tkhruni, F. N., Aghajanyan, A. E., Balabekyan, T. R., Khachatryan, T. V., & Karapetyan, K. J. (2020). Characteristic of bacteriocins of Lactobacillus rhamnosus BTK 20-12 potential probiotic strain. Probiotics and Antimicrobial Proteins, 12(2), 716-724. http://dx.doi.org/10.1007/s12602-019-09569-y PMid:31338788.
  » http://dx.doi.org/10.1007/s12602-019-09569-y
• Todorov, S. D., Franco, B. D. G. M., & Tagg, J. R. (2019). Bacteriocins of Gram-positive bacteria having activity spectra extending beyond closely-related species. Beneficial Microbes, 10(3), 315-328. http://dx.doi.org/10.3920/BM2018.0126 PMid:30773930.
  » http://dx.doi.org/10.3920/BM2018.0126
• Trejo-González, L., Gutiérrez-Carrillo, A. E., Rodríguez-Hernández, A. I., López-Cuellar, M. R., & Chavarría-Hernández, N. (2021). Bacteriocins produced by LAB isolated from cheeses within the period 2009-2021: a review. Probiotics and Antimicrobial Proteins, 14(2), 238-251. PMid:34342858.
• Veettil, V. N., & Chitra, V. (2022). Review lantibiotics of milk isolates: a short review on characterization and potential applications. Journal of Microbiology, Biotechnology and Food Sciences, 11(4), e3702. http://dx.doi.org/10.55251/jmbfs.3702
  » http://dx.doi.org/10.55251/jmbfs.3702
• Wang, Q., Yang, L., Feng, K., Li, H., Deng, Z., & Liu, J. (2021). Promote lactic acid production from food waste fermentation using biogas slurry recirculation. Bioresource Technology, 337, 125393. http://dx.doi.org/10.1016/j.biortech.2021.125393 PMid:34120058.
  » http://dx.doi.org/10.1016/j.biortech.2021.125393
• Yaghoubi, A., Khazaei, M., Jalili, S., Hasanian, S. M., Avan, A., Soleimanpour, S., & Cho, W. C. (2020). Bacteria as a double-action sword in cancer. Biochimica et Biophysica Acta-Reviews on Cancer, 1874(1), 188388. http://dx.doi.org/10.1016/j.bbcan.2020.188388 PMid:32589907.
  » http://dx.doi.org/10.1016/j.bbcan.2020.188388
• Yang, E., Fan, L., Yan, J., Jiang, Y., Doucette, C., Fillmore, S., & Walker, B. (2018). Influence of culture media, pH and temperature on growth and bacteriocin production of bacteriocinogenic lactic acid bacteria. AMB Express, 8(1), 10. http://dx.doi.org/10.1186/s13568-018-0536-0 PMid:29368243.
  » http://dx.doi.org/10.1186/s13568-018-0536-0
• Yi, Y., Li, P., Zhao, F., Zhang, T., Shan, Y., Wang, X., Liu, B., Chen, Y., Zhao, X., & Lü, X. (2022). Current status and potentiality of class II bacteriocins from lactic acid bacteria: structure, mode of action and applications in the food industry. Trends in Food Science & Technology, 120, 387-401. http://dx.doi.org/10.1016/j.tifs.2022.01.018
  » http://dx.doi.org/10.1016/j.tifs.2022.01.018
• Zimina, M., Babich, O., Prosekov, A., Sukhikh, S., Ivanova, S., Shevchenko, M., & Noskova, S. (2020). Overview of global trends in classification, methods of preparation and application of bacteriocins. Antibiotics, 9(9), 553. http://dx.doi.org/10.3390/antibiotics9090553 PMid:32872235.
  » http://dx.doi.org/10.3390/antibiotics9090553
• Zou, J., Jiang, H., Cheng, H., Fang, J., & Huang, G. (2018). Strategies for screening, purification and characterization of bacteriocins. International Journal of Biological Macromolecules, 117, 781-789. http://dx.doi.org/10.1016/j.ijbiomac.2018.05.233 PMid:29870810.
  » http://dx.doi.org/10.1016/j.ijbiomac.2018.05.233

Publication Dates

• Publication in this collection
  16 Jan 2023
• Date of issue
  2023

History

• Received
  29 Oct 2022
• Accepted
  11 Dec 2022